Cited by 209Phytochemicals and Antioxidant ActivitiesFood Chemistry and Fat AnalysisNutritional Studies and Diet

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Effect of cocoa powder on the modulation of inflammatory biomarkers in patients at high risk of cardiovascular disease

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Monagas, Maria, Khan, Nasiruddin, Andres-Lacueva, Cristina, Casas, Rosa, Urpí-Sardà, Mireia, Llorach, Rafael, Lamuela-Raventós, Rosa Maria, Estruch, Ramón·2009·The American Journal of Clinical Nutrition

DOI 10.3945/ajcn.2009.27716

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Abstract

Background Epidemiologic studies have suggested that flavonoid intake plays a critical role in the prevention of coronary heart disease. Because atherosclerosis is considered a low-grade inflammatory disease, some feeding trials have analyzed the effects of cocoa (an important source of flavonoids) on inflammatory biomarkers, but the results have been controversial.Objective The objective was to evaluate the effects of chronic cocoa consumption on cellular and serum biomarkers related to atherosclerosis in high-risk patients.Design Forty-two high-risk volunteers (19 men and 23 women; mean +/- SD age: 69.7 +/- 11.5 y) were included in a randomized crossover feeding trial. All subjects received 40 g cocoa powder with 500 mL skim milk/d (C+M) or only 500 mL skim milk/d (M) for 4 wk. Before and after each intervention period, cellular and serum inflammatory biomarkers related to atherosclerosis were evaluated.Results Adherence to the dietary protocol was excellent. No significant changes in the expression of adhesion molecules on T lymphocyte surfaces were found between the C+M and M groups. However, in monocytes, the expression of VLA-4, CD40, and CD36 was significantly lower (P = 0.005, 0.028, and 0.001, respectively) after C+M intake than after M intake. In addition, serum concentrations of the soluble endothelium-derived adhesion molecules P-selectin and intercellular adhesion molecule-1 were significantly lower (both P = 0.007) after C+M intake than after M intake.Conclusions These results suggest that the intake of cocoa polyphenols may modulate inflammatory mediators in patients at high risk of cardiovascular disease. These antiinflammatory effects may contribute to the overall benefits of cocoa consumption against atherosclerosis. This trial was registered in the Current Controlled Trials at London, International Standard Randomized Controlled Trial Number, at controlled-trials.com as ISRCTN75176807.

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Colorimetry of Total Phenolics with Phosphomolybdic-Phosphotungstic Acid Reagents
Singleton, V. L., & Rossi, J. A. (1965) · American Journal of Enology and Viticulture · doi:10.5344/ajev.1965.16.3.144 · Cited by 24,852
Effects of a Mediterranean-Style Diet on Cardiovascular Risk Factors: A Randomized Trial
Estruch, R., Martínez-González, M. Á., Corella, D., Salas-Salvadó, J., Ruiz-Gutiérrez, V., Covas, M. I., Fiol, M., Gómez-Gracia, E., López-Sabater, M. C., Vinyoles, E., et al. (2006) · Annals of Internal Medicine · doi:10.7326/0003-4819-145-1-200607040-00004 · Cited by 1,704
Inflammation and cardiovascular disease mechanisms
Libby, P. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.2.456s · Cited by 1,114
Endothelial cell functions
Michiels, C. (2003) · Journal of Cellular Physiology · doi:10.1002/jcp.10333 · Cited by 828
Cocoa Has More Phenolic Phytochemicals and a Higher Antioxidant Capacity than Teas and Red Wine
Lee, K. W., Kim, Y. J., Lee, H. J., & Lee, C. Y. (2003) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0344385 · Cited by 748
Plasma antioxidants from chocolate
Serafini, M., Bugianesi, R., Maiani, G., Valtuena, S., De Santis, S., & Crozier, A. (2003) · Nature · doi:10.1038/4241013a · Cited by 539
Effects of cocoa powder and dark chocolate on LDL oxidative susceptibility and prostaglandin concentrations in humans
Wan, Y., Vinson, J. A., Etherton, T. D., Proch, J., Lazarus, S. A., & Kris‐Etherton, P. M. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/74.5.596 · Cited by 341
Cocoa and health: a decade of research
Cooper, K., Donovan, J. L., Waterhouse, A. L., & Williamson, G. (2007) · British Journal Of Nutrition · doi:10.1017/s0007114507795296 · Cited by 302
Chocolate and Prevention of Cardiovascular Disease: A Systematic Review
Ding, E. L., Hutfless, S. M., Ding, X., & Girotra, S. R. (2006) · Nutrition & Metabolism · doi:10.1186/1743-7075-3-2 · Cited by 275
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Mursu, J., Voutilainen, S., Nurmi, T., Rissanen, T. H., Virtanen, J. K., Kaikkonen, J., Nyyssönen, K., & Salonen, J. T. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.06.002 · Cited by 272
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Baba, S., Osakabe, N., Kato, Y., Natsume, M., Yasuda, A., Kido, T., Fukuda, K., Muto, Y., & Kondo, K. N. (2007) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/85.3.709 · Cited by 247
Use of a three-day estimated food record, a 72-hour recall and a food-frequency questionnaire for dietary assessment in a Mediterranean Spanish population
Schröder, H., Covas, M.-I., Marrugat, J., Vila, J., PENA, A., Alcantara, M., & Masià, R. (2001) · Clinical Nutrition · doi:10.1054/clnu.2001.0460 · Cited by 238
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Stalmach, A., Troufflard, S., Serafini, M., & Crozier, A. (2008) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.200800169 · Cited by 218
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Sanbongi, C., Suzuki, N., & Sakane, T. (1997) · Cellular Immunology · doi:10.1006/cimm.1997.1109 · Cited by 210
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Mathur, S., Grundy, S. M., Devaraj, S., & Jialal, I. (2002) · The Journal of Nutrition · doi:10.1093/jn/132.12.3663 · Cited by 178
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Wang, J. F., Villablanca, A. C., Polagruto, J. A., Lee, L., Holt, R. R., Schrader, H. R., Ensunsa, J. L., Steinberg, F. M., Schmitz, H. H., & Keen, C. L. (2006) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-200606001-00013 · Cited by 153
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Mullen, W., Borges, G., Donovan, J. L., Edwards, C. A., Serafini, M., Lean, M. E. J., & Crozier, A. (2009) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.27339 · Cited by 121
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Rapid Liquid Chromatography Tandem Mass Spectrometry Assay To Quantify Plasma (−)-Epicatechin Metabolites after Ingestion of a Standard Portion of Cocoa Beverage in Humans
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Cardioprotective effects of chocolate and almond consumption in healthy women
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Effect of Cocoa Flavanols and Their Related Oligomers on the Secretion of Interleukin-5 in Peripheral Blood Mononuclear Cells
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Effect ofTheobroma cacaoflavonoids on immune activation of a lymphoid cell line
Ramiro‐Puig, E., Franch, À., Castellote, C., Andrés‐Lacueva, C., Izquierdo-Pulido, M., & Castell, M. (2005) · British Journal Of Nutrition · doi:10.1079/bjn20051443 · Cited by 59
Cocoa Flavonols and Procyanidins Promote Transforming Growth Factor-β 1 Homeostasis in Peripheral Blood Mononuclear Cells 1
Mao, T. K., de Water, J. V., Keen, C. L., Schmitz, H. H., & Gershwin, M. E. (2003) · Experimental Biology and Medicine · doi:10.1177/153537020322800113 · Cited by 57
Quality Assessment of Commercial Dietary Antioxidant Products From Vitis vinifera L. Grape Seeds
Monagas, M., Hernández‐Ledesma, B., Garrido, I., Martín-Álvarez, P. J., Gómez‐Cordovés, C., & Bartolomé, B. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5302_13 · Cited by 41
Upregulated Expression of VLA Proteins and CD29 in Peripheral Blood Lymphocytes of Chronic Alcoholics Without Ethanol-Related Diseases
Sacanella, E., Estruch, R., Gayà, A., Ferrer, K., Fernández-Solá, J., Alonso, J. R., Nicolás, J. M., & Urbano-Márquez, A. (1999) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1999.tb04124.x · Cited by 17

Research works printed but not linked: 1

Ribéreau-Gayon, 1966, Dósage des tannins du vin rouges et determination du leur structure., [Doses of tannins in red wine and analysis of their structure.] Chim Anal, 48, 188

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Authors: Monagas, M., Khan, N., Andres-Lacueva, C., Casas, R., Urpí-Sardà, M., Llorach, R., Lamuela-Raventós, R. M., & Estruch, R.
Affiliations: Instituto de Salud Carlos III (ES)
Corresponding author: Estruch, Ramón
ORCID: Khan, Nasiruddin
Casas, Rosa
Urpí-Sardà, Mireia
Lamuela-Raventós, Rosa Maria
Estruch, Ramón
Venue: The American Journal of Clinical Nutrition
Publisher: Elsevier BV
Published: 2009-11
Volume: 90
Issue: 5
Pages: 1144-1150
ISSN: 0002-9165 (ISSN-L)
DOI: 10.3945/ajcn.2009.27716
OpenAlex: W1964861389
Cited by: 209
References: 41
Citations by year: 2026: 3 · 2025: 3 · 2024: 5 · 2023: 4 · 2022: 7 · 2021: 7 · 2020: 10 · 2019: 13 · 2018: 11 · 2017: 15 · 2016: 22 · 2015: 14 · 2014: 14 · 2013: 31 · 2012: 24
FWCI: 10.46
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 4862 d)
Locations: American Journal of Clinical Nutrition (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion, other-oa)
Dipòsit Digital de la Universitat de Barcelona (Universitat de Barcelona) (submittedVersion, public-domain)
RECERCAT (Consorci de Serveis Universitaris de Catalunya) (submittedVersion)
Topics: Health Sciences › Medicine › Biochemistry (medical) › Phytochemicals and Antioxidant Activities
Life Sciences › Agricultural and Biological Sciences › Food Science › Food Chemistry and Fat Analysis
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
Keywords: cocoa powder, cocoa polyphenols, flavonoids, atherosclerosis, inflammation, inflammatory markers, cardiovascular risk, monocytes, adhesion molecules, VLA-4, CD40, CD36, P-selectin, ICAM-1, T cells, dietary intervention
MeSH terms: Aged, Aged, 80 and over, Blood Pressure, Body Weight, Cacao, Cardiovascular Diseases, Coronary Disease, Female, Flavonoids, Humans, Inflammation, Leukocytes, Mononuclear, Male, Middle Aged, Monocytes, Obesity, Risk Factors, Smoking, T-Lymphocytes, Immunophenotyping, Patient Selection, Cross-Over Studies

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Effect of cocoa powder on the modulation of inflammatory biomarkers in patients at high risk of cardiovascular disease

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